Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage
Abstract
Triose phosphate utilization (TPU)-limited photosynthesis occurs when carbon export from the Calvin-Benson cycle cannot keep pace with carbon inputs and processing. This condition is poorly constrained by observations but may become an increasingly important driver of global carbon cycling under future climate scenarios. However, the consequences of including or omitting TPU limitation in models have seldom been quantified. In this work, we assess the impact of changing the representation of TPU limitation on leaf- and global-scale processes. At the leaf scale, TPU limits photosynthesis at cold temperatures, high CO2 concentrations, and high light levels. Consistent with leaf-scale results, global simulations using the Community Land Model version 4.5 illustrate that the standard representation of TPU limits carbon gain under present day and future conditions, most consistently at high latitudes. If the assumed TPU limitation is doubled, further restricting photosynthesis, terrestrial ecosystem carbon pools are reduced by 9 Pg by 2100 under a business-as-usual scenario. The impact of TPU limitation on global terrestrial carbon gain suggests that CO2 concentrations may increase more than expected if models omit TPU limitation, and highlights the need to better understand when TPU limitation is important, including variation among different plant types and acclimation to temperature andmore »
- Authors:
- Publication Date:
- Research Org.:
- Univ. of Michigan, Ann Arbor, MI (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States); Michigan State Univ., East Lansing, MI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); USDA; National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES); National Institute of Food and Agriculture (NIFA)
- OSTI Identifier:
- 1459720
- Alternate Identifier(s):
- OSTI ID: 1459167; OSTI ID: 1603664
- Report Number(s):
- BNL-206806-2018-JAAM
Journal ID: ISSN 1748-9326
- Grant/Contract Number:
- FC03-97ER62402/A010; FG02-91ER2002; SC0012704; SC0012972; 2015-67003-23485; FC03-97ER62402/377 A010; 2015-67003-23489; 1049033; 1000026; FG02-91ER20021
- Resource Type:
- Published Article
- Journal Name:
- Environmental Research Letters
- Additional Journal Information:
- Journal Name: Environmental Research Letters Journal Volume: 13 Journal Issue: 7; Journal ID: ISSN 1748-9326
- Publisher:
- IOP Publishing
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 54 ENVIRONMENTAL SCIENCES; triose phosphate utilization; terrestrial carbon storage; photosynthesis models
Citation Formats
Lombardozzi, Danica L., Smith, Nicholas G., Cheng, Susan J., Dukes, Jeffrey S., Sharkey, Thomas D., Rogers, Alistair, Fisher, Rosie, and Bonan, Gordon B. Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage. United Kingdom: N. p., 2018.
Web. doi:10.1088/1748-9326/aacf68.
Lombardozzi, Danica L., Smith, Nicholas G., Cheng, Susan J., Dukes, Jeffrey S., Sharkey, Thomas D., Rogers, Alistair, Fisher, Rosie, & Bonan, Gordon B. Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage. United Kingdom. https://doi.org/10.1088/1748-9326/aacf68
Lombardozzi, Danica L., Smith, Nicholas G., Cheng, Susan J., Dukes, Jeffrey S., Sharkey, Thomas D., Rogers, Alistair, Fisher, Rosie, and Bonan, Gordon B. Tue .
"Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage". United Kingdom. https://doi.org/10.1088/1748-9326/aacf68.
@article{osti_1459720,
title = {Triose phosphate limitation in photosynthesis models reduces leaf photosynthesis and global terrestrial carbon storage},
author = {Lombardozzi, Danica L. and Smith, Nicholas G. and Cheng, Susan J. and Dukes, Jeffrey S. and Sharkey, Thomas D. and Rogers, Alistair and Fisher, Rosie and Bonan, Gordon B.},
abstractNote = {Triose phosphate utilization (TPU)-limited photosynthesis occurs when carbon export from the Calvin-Benson cycle cannot keep pace with carbon inputs and processing. This condition is poorly constrained by observations but may become an increasingly important driver of global carbon cycling under future climate scenarios. However, the consequences of including or omitting TPU limitation in models have seldom been quantified. In this work, we assess the impact of changing the representation of TPU limitation on leaf- and global-scale processes. At the leaf scale, TPU limits photosynthesis at cold temperatures, high CO2 concentrations, and high light levels. Consistent with leaf-scale results, global simulations using the Community Land Model version 4.5 illustrate that the standard representation of TPU limits carbon gain under present day and future conditions, most consistently at high latitudes. If the assumed TPU limitation is doubled, further restricting photosynthesis, terrestrial ecosystem carbon pools are reduced by 9 Pg by 2100 under a business-as-usual scenario. The impact of TPU limitation on global terrestrial carbon gain suggests that CO2 concentrations may increase more than expected if models omit TPU limitation, and highlights the need to better understand when TPU limitation is important, including variation among different plant types and acclimation to temperature and CO2.},
doi = {10.1088/1748-9326/aacf68},
journal = {Environmental Research Letters},
number = 7,
volume = 13,
place = {United Kingdom},
year = {Tue Jul 10 00:00:00 EDT 2018},
month = {Tue Jul 10 00:00:00 EDT 2018}
}
https://doi.org/10.1088/1748-9326/aacf68
Web of Science
Works referenced in this record:
Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway
journal, December 2017
- Busch, Florian A.; Sage, Rowan F.; Farquhar, Graham D.
- Nature Plants, Vol. 4, Issue 1
Predicting leaf Physiology from Simple Plant and Climate Attributes: a Global Glopnet Analysis
journal, October 2007
- Reich, Peter B.; Wright, Ian J.; Lusk, Christopher H.
- Ecological Applications, Vol. 17, Issue 7
TRY - a global database of plant traits: TRY - A GLOBAL DATABASE OF PLANT TRAITS
journal, June 2011
- Kattge, J.; DÍAz, S.; Lavorel, S.
- Global Change Biology, Vol. 17, Issue 9
Limitation to Photosynthesis in Water-stressed Leaves: Stomata vs. Metabolism and the Role of ATP
journal, June 2002
- Lawlor, D. W.
- Annals of Botany, Vol. 89, Issue 7
Ozone exposure causes a decoupling of conductance and photosynthesis: implications for the Ball-Berry stomatal conductance model
journal, January 2012
- Lombardozzi, Danica; Sparks, Jed P.; Bonan, Gordon
- Oecologia, Vol. 169, Issue 3
Acclimation of Photosynthesis to Elevated CO 2 in Five C 3 Species
journal, February 1989
- Sage, Rowan F.; Sharkey, Thomas D.; Seemann, Jeffrey R.
- Plant Physiology, Vol. 89, Issue 2
The Effect of Leaf Nitrogen and Temperature on the CO2 Response of Photosynthesis in the C3 Dicot MChenopodium album L
journal, January 1990
- Sage, Rf; Sharkey, Td; Pearcy, Rw
- Functional Plant Biology, Vol. 17, Issue 2
Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer
journal, April 1991
- Collatz, G. James; Ball, J. Timothy; Grivet, Cyril
- Agricultural and Forest Meteorology, Vol. 54, Issue 2-4
Optimal allocation of leaf-level nitrogen: Implications for covariation of V cmax and J max and photosynthetic downregulation: COVARIATION OF V cmax AND J max
journal, September 2016
- Quebbeman, J. A.; Ramirez, J. A.
- Journal of Geophysical Research: Biogeosciences, Vol. 121, Issue 9
Improving canopy processes in the Community Land Model version 4 (CLM4) using global flux fields empirically inferred from FLUXNET data
journal, January 2011
- Bonan, Gordon B.; Lawrence, Peter J.; Oleson, Keith W.
- Journal of Geophysical Research, Vol. 116, Issue G2
A Revised Land Surface Parameterization (SiB2) for Atmospheric GCMS. Part I: Model Formulation
journal, April 1996
- Sellers, P. J.; Randall, D. A.; Collatz, G. J.
- Journal of Climate, Vol. 9, Issue 4
Toward a Mechanistic Modeling of Nitrogen Limitation on Vegetation Dynamics
journal, May 2012
- Xu, Chonggang; Fisher, Rosie; Wullschleger, Stan D.
- PLoS ONE, Vol. 7, Issue 5
Reconciling leaf physiological traits and canopy flux data: Use of the TRY and FLUXNET databases in the Community Land Model version 4: COMMUNITY LAND MODEL CANOPY SCALING
journal, June 2012
- Bonan, Gordon B.; Oleson, Keith W.; Fisher, Rosie A.
- Journal of Geophysical Research: Biogeosciences, Vol. 117, Issue G2
Comprehensive ecosystem model-data synthesis using multiple data sets at two temperate forest free-air CO 2 enrichment experiments: Model performance at ambient CO 2 concentration : FACE MODEL-DATA SYNTHESIS
journal, May 2014
- Walker, Anthony P.; Hanson, Paul J.; De Kauwe, Martin G.
- Journal of Geophysical Research: Biogeosciences, Vol. 119, Issue 5
The response of photosynthesis and stomatal conductance to rising [CO 2 ]: mechanisms and environmental interactions : Photosynthesis and stomatal conductance responses to rising [CO
journal, January 2007
- Ainsworth, Elizabeth A.; Rogers, Alistair
- Plant, Cell & Environment, Vol. 30, Issue 3
The sensitivity of photosynthesis to O 2 and CO 2 concentration identifies strong Rubisco control above the thermal optimum
journal, October 2016
- Busch, Florian A.; Sage, Rowan F.
- New Phytologist, Vol. 213, Issue 3
Coupled Photosynthesis-Stomatal Conductance Model for Leaves of C4 Plants
journal, January 1992
- Collatz, Gj; Ribas-Carbo, M.; Berry, Ja
- Functional Plant Biology, Vol. 19, Issue 5
Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling
journal, May 2012
- Bauerle, W. L.; Oren, R.; Way, D. A.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 22
Evaluating the Land and Ocean Components of the Global Carbon Cycle in the CMIP5 Earth System Models
journal, September 2013
- Anav, A.; Friedlingstein, P.; Kidston, M.
- Journal of Climate, Vol. 26, Issue 18
Phosphorus recycling in photorespiration maintains high photosynthetic capacity in woody species: Phosphorus recycling in photorespiration
journal, January 2015
- Ellsworth, David S.; Crous, Kristine Y.; Lambers, Hans
- Plant, Cell & Environment, Vol. 38, Issue 6
Reliable estimation of biochemical parameters from C3 leaf photosynthesis-intercellular carbon dioxide response curves: Estimating FvCB model parameters
journal, June 2010
- Gu, Lianhong; Pallardy, Stephen G.; Tu, Kevin
- Plant, Cell & Environment, Vol. 33, Issue 11
Global Carbon Budget 2016
journal, January 2016
- Le Quéré, Corinne; Andrew, Robbie M.; Canadell, Josep G.
- Earth System Science Data, Vol. 8, Issue 2
What gas exchange data can tell us about photosynthesis: Gas exchange data and photosynthesis
journal, December 2015
- Sharkey, Thomas D.
- Plant, Cell & Environment, Vol. 39, Issue 6
Improved temperature response functions for models of Rubisco-limited photosynthesis
journal, February 2001
- Bernacchi, C. J.; Singsaas, E. L.; Pimentel, C.
- Plant, Cell and Environment, Vol. 24, Issue 2
Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum
journal, September 2014
- Dahal, K.; Wang, J.; Martyn, G. D.
- PLANT PHYSIOLOGY, Vol. 166, Issue 3
Climate System Response to External Forcings and Climate Change Projections in CCSM4
journal, June 2012
- Meehl, Gerald A.; Washington, Warren M.; Arblaster, Julie M.
- Journal of Climate, Vol. 25, Issue 11
Global-scale environmental control of plant photosynthetic capacity
journal, December 2015
- Ali, Ashehad A.; Xu, Chonggang; Rogers, Alistair
- Ecological Applications, Vol. 25, Issue 8
Temperature acclimation of photosynthesis and respiration: A key uncertainty in the carbon cycle-climate feedback: PHYSIOLOGICAL TEMPERATURE ACCLIMATION
journal, October 2015
- Lombardozzi, Danica L.; Bonan, Gordon B.; Smith, Nicholas G.
- Geophysical Research Letters, Vol. 42, Issue 20
Plant adaptation or acclimation to rising CO 2 ? Insight from first multigenerational RNA-Seq transcriptome
journal, August 2016
- Watson-Lazowski, Alexander; Lin, Yunan; Miglietta, Franco
- Global Change Biology, Vol. 22, Issue 11
Biochemical Limitations to Carbon Assimilation in C 3 Plants—A Retrospective Analysis of the A/C i Curves from 109 Species
journal, January 1993
- Wullschleger, Stan D.
- Journal of Experimental Botany, Vol. 44, Issue 5
Carbon–Concentration and Carbon–Climate Feedbacks in CMIP5 Earth System Models
journal, August 2013
- Arora, Vivek K.; Boer, George J.; Friedlingstein, Pierre
- Journal of Climate, Vol. 26, Issue 15
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
journal, June 1980
- Farquhar, G. D.; von Caemmerer, S.; Berry, J. A.
- Planta, Vol. 149, Issue 1
Triose phosphate use limitation of photosynthesis: short-term and long-term effects
journal, November 2015
- Yang, Jennifer T.; Preiser, Alyssa L.; Li, Ziru
- Planta, Vol. 243, Issue 3
Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species
journal, September 2007
- Kattge, Jens; Knorr, Wolfgang
- Plant, Cell & Environment, Vol. 30, Issue 9
The use and misuse of V c,max in Earth System Models
journal, April 2013
- Rogers, Alistair
- Photosynthesis Research, Vol. 119, Issue 1-2
Improving the representation of radiation interception and photosynthesis for climate model applications
journal, July 2007
- Mercado, Lina M.; Huntingford, Chris; Gash, John H. C.
- Tellus B, Vol. 59, Issue 3
A global scale mechanistic model of photosynthetic capacity (LUNA V1.0)
journal, January 2016
- Ali, A. A.; Xu, C.; Rogers, A.
- Geoscientific Model Development, Vol. 9, Issue 2
Towards a universal model for carbon dioxide uptake by plants
journal, September 2017
- Wang, Han; Prentice, I. Colin; Keenan, Trevor F.
- Nature Plants, Vol. 3, Issue 9
Reducing uncertainty in projections of terrestrial carbon uptake
journal, April 2017
- Lovenduski, Nicole S.; Bonan, Gordon B.
- Environmental Research Letters, Vol. 12, Issue 4
Modeling Global and Regional Net Primary Production under Elevated Atmospheric CO 2 : On a Potential Source of Uncertainty
journal, January 2006
- El Maayar, Mustapha; Ramankutty, Navin; Kucharik, Christopher J.
- Earth Interactions, Vol. 10, Issue 2
A roadmap for improving the representation of photosynthesis in Earth system models
journal, November 2016
- Rogers, Alistair; Medlyn, Belinda E.; Dukes, Jeffrey S.
- New Phytologist, Vol. 213, Issue 1
Mild Water Stress of Phaseolus vulgaris Plants Leads to Reduced Starch Synthesis and Extractable Sucrose Phosphate Synthase Activity
journal, April 1989
- Vassey, Terry L.; Sharkey, Thomas D.
- Plant Physiology, Vol. 89, Issue 4
Quantifying photosynthetic capacity and its relationship to leaf nitrogen content for global-scale terrestrial biosphere models
journal, April 2009
- Kattge, Jens; Knorr, Wolfgang; Raddatz, Thomas
- Global Change Biology, Vol. 15, Issue 4
Works referencing / citing this record:
Critical review: incorporating the arrangement of mitochondria and chloroplasts into models of photosynthesis and carbon isotope discrimination
journal, April 2019
- Ubierna, Nerea; Cernusak, Lucas A.; Holloway-Phillips, Meisha
- Photosynthesis Research, Vol. 141, Issue 1
Beyond Static Benchmarking: Using Experimental Manipulations to Evaluate Land Model Assumptions
journal, October 2019
- Wieder, William R.; Lawrence, David M.; Fisher, Rosie A.
- Global Biogeochemical Cycles, Vol. 33, Issue 10
Changes in Wood Biomass and Crop Yields in Response to Projected CO 2 , O 3 , Nitrogen Deposition, and Climate
journal, October 2018
- Lombardozzi, Danica L.; Bonan, Gordan B.; Levis, Samuel
- Journal of Geophysical Research: Biogeosciences, Vol. 123, Issue 10
Model Structure and Climate Data Uncertainty in Historical Simulations of the Terrestrial Carbon Cycle (1850–2014)
journal, October 2019
- Bonan, Gordon B.; Lombardozzi, Danica L.; Wieder, William R.
- Global Biogeochemical Cycles, Vol. 33, Issue 10
Triose phosphate utilization and beyond: from photosynthesis to end product synthesis
journal, March 2019
- McClain, Alan M.; Sharkey, Thomas D.
- Journal of Experimental Botany, Vol. 70, Issue 6
Is triose phosphate utilization involved in the feedback inhibition of photosynthesis in rice under conditions of sink limitation?
journal, July 2019
- Fabre, Denis; Yin, Xinyou; Dingkuhn, Michael
- Journal of Experimental Botany, Vol. 70, Issue 20
Is triose phosphate utilization important for understanding photosynthesis?
journal, October 2019
- Sharkey, Thomas D.
- Journal of Experimental Botany, Vol. 70, Issue 20
Using multirate rapid A / C i curves as a tool to explore new questions in the photosynthetic physiology of plants
journal, January 2019
- Stinziano, Joseph R.; Adamson, Rachael K.; Hanson, David T.
- New Phytologist, Vol. 222, Issue 2
No evidence for triose phosphate limitation of light‐saturated leaf photosynthesis under current atmospheric CO 2 concentration
journal, August 2019
- Kumarathunge, Dushan P.; Medlyn, Belinda E.; Drake, John E.
- Plant, Cell & Environment, Vol. 42, Issue 12
Genotypic variation in source and sink traits affects the response of photosynthesis and growth to elevated atmospheric CO 2
journal, December 2019
- Fabre, Denis; Dingkuhn, Michael; Yin, Xinyou
- Plant, Cell & Environment, Vol. 43, Issue 3
Decadal fates and impacts of nitrogen additions on temperate forest carbon storage: a data–model comparison
journal, January 2019
- Cheng, Susan J.; Hess, Peter G.; Wieder, William R.
- Biogeosciences, Vol. 16, Issue 13
The biophysics, ecology, and biogeochemistry of functionally diverse, vertically and horizontally heterogeneous ecosystems: the Ecosystem Demography model, version 2.2 – Part 1: Model description
journal, January 2019
- Longo, Marcos; Knox, Ryan G.; Medvigy, David M.
- Geoscientific Model Development, Vol. 12, Issue 10